Recoding of stop codons expands the metabolic potential of two novel Asgardarchaeota lineages

Abstract

Asgardarchaeota have been proposed as the closest living relatives to eukaryotes, and a total of 72 metagenome-assembled genomes (MAGs) representing six primary lineages in this archaeal phylum have thus far been described. These organisms are predicted to be fermentative heterotrophs contributing to carbon cycling in sediment ecosystems. Here, we double the genomic catalogue of Asgardarchaeota by obtaining 71 MAGs from a range of habitats around the globe, including the deep subsurface, brackish shallow lakes, and geothermal spring sediments. Phylogenomic inferences followed by taxonomic rank normalisation confirmed previously established Asgardarchaeota classes and revealed four additional lineages, two of which were consistently recovered as monophyletic classes. We therefore propose the names Candidatus Sifarchaeia class nov. and Ca. Jordarchaeia class nov., derived from the gods Sif and Jord in Norse mythology. Metabolic inference suggests that both classes represent hetero-organotrophic acetogens, which also have the ability to utilise methyl groups such as methylated amines, with acetate as the probable end product in remnants of a methanogen-derived core metabolism. This inferred mode of energy conservation is predicted to be enhanced by genetic code expansions, i.e., stop codon recoding, allowing the incorporation of the rare 21st and 22nd amino acids selenocysteine (Sec) and pyrrolysine (Pyl). We found Sec recoding in Jordarchaeia and all other Asgardarchaeota classes, which likely benefit from increased catalytic activities of Sec-containing enzymes. Pyl recoding, on the other hand, is restricted to Sifarchaeia in the Asgardarchaeota, making it the first reported non-methanogenic archaeal lineage with an inferred complete Pyl machinery, likely providing members of this class with an efficient mechanism for methylamine utilisation. Furthermore, we identified enzymes for the biosynthesis of ester-type lipids, characteristic of bacteria and eukaryotes, in both newly described classes, supporting the hypothesis that mixed ether-ester lipids are a shared feature among Asgardarchaeota.

Indirect Routes to Aminoacyl-tRNA: The Diversity of Prokaryotic Cysteine Encoding Systems

“…Interestingly, in a small lineage of Sifarchaeia archaea ( Sun et al, 2021 ) possessing SepRS-SepCysS-SepCysSn, their PSTK and aSelB ORFs are split by a stop codon ( Figure 9A ). Thus, erroneous conversion of Sep-tRNA Sec to Cys-tRNA Sec might be acceptable to these archaea to some extent.…”

Editorial: Ecology, Metabolism and Evolution of Archaea-Perspectives From Proceedings of the International Workshop on Geo-Omics of Archaea

“…At the same time there is a need to distinguish between genomic potential for physiological traits and bona fide expressed traits in situ or in cultured cells. For example, Sun et al (2021) and Villanueva et al (2021) report exciting collections of genes from uncultured archaea that suggest the ability for coexistence of archaeal and bacterial lipids in the same cell. But do they really synthesize those lipids?…”

The expanding Asgard archaea and their elusive relationships with Eukarya

“…Schematic representation of the known diversity of the Asgard archaea including the recently published lineages. In this schema, we indicate in orange and red the newly discovered lineages introduced in the two publications of Liu et al 13 and Xie et al 14 , respectively, and in grey new lineages not present in these publications corresponding to the Sifarchaea 12 , the Jordarchaeia 16 and Asgard Lake Cootharaba 16 . The schema was designed combining the trees of all these publications.…”

“…The number of proposed Asgard phyla has continuously increased in recent years, from 1 in 2015 (Lokiarchaeota) to 18 in late 2021 (Figure 2) 1,2,10–16 . In a recent study, Liu et al 13 described six new Asgard phyla from an analysis of 75 metagenome‐assembled genomes (MAGs), while three additional phyla were described by Xie et al 14 from an analysis of 128 new MAGs.…”

“…Rinke and colleagues recently proposed to consider the whole Asgard clade as a single phylum and the various Asgard lineages either as families or orders, with some of them being grouped in classes 16 . Since it is still an ongoing debate at the time of writing this review 18 , we will here use the more neutral term “lineage” for the various subgroups of Asgards (e.g., Heimdall lineage for Heimdallarchaeota/ales).…”